Abstract
The increasing urbanisation of the natural environment affects species differently. While most species cannot cope with these human impacts, others can persist or may even be favoured in these anthropogenic ecosystems. Among the different urban-adapted wildlife species, the populations of different species of opportunistic gulls have increased in urban areas and some have established breeding populations at a global scale. Although the ecology of these predators is relatively well-known in their natural environment, accurate knowledge about their urban ecology is very scarce. Here, we investigated the foraging ecology (habitat use, spatial movements and feeding) of an urban population of yellow-legged gulls (Larus michahellis) inhabiting the city of Barcelona (north-eastern Spain). We examined the diet of this urban population by analysing the stomach contents of chicks distributed throughout the urban area of Barcelona. The foraging movements of breeding gulls were investigated using GPS devices and habitat landscape information. The results show that this urban population of yellow-legged gull exploits different food resources, highlighting the consumption of urban birds and marine resources from fishery discards. In line with the diet results, GPS tracking data indicated that although yellow-legged gulls were able to use different types of habitats close to the city, they mainly foraged in urban and fishing port areas. In conclusion, yellow-legged gulls have adapted to exploit the food resources associated with urban environments. This study provides useful information to discuss management options measures to control the yellow-legged gull populations nesting in urban areas.
Similar content being viewed by others
References
Alm EW, Daniels-Witt QR, Learman DR, Ryu H, Jordan DW, Gehring TM, Santo Domingo J (2018) Potential for gulls to transport bacteria from human waste sites to beaches. Sci Total Environ 615:123–130. https://doi.org/10.1016/j.scitotenv.2017.09.232
Anderson M, Gorley R, Clarke K (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E Ltd, Plymouthm UK
Anton M, Herrando S, García D, et al (2017) Atles dels ocells nidificants de Barcelona, 1st Ed. Edicions de la Universitat de Barcelona. Barcelona, Spain
Arcos J (2001) Foraging ecology of seabirds at sea: significance of commercial fisheries in the Northwest Mediterranean. PhD Thesis. Departament de Biologia Animal. Universitat de Barcelona, Spain. Universitat de Barcelona
Arizaga J, Aldalur A, Herrero A, Cuadrado JF, Díez E, Crespo A (2014) Foraging distances of a resident yellow-legged gull (Larus michahellis) population in relation to refuse management on a local scale. Eur J Wildl Res 60:171–175. https://doi.org/10.1007/s10344-013-0761-4
Auman H. J, Meathrel C. E, Richardson A (2008) Supersize me: does anthropogenic food change the body condition of silver gulls? A comparison between urbanized and remote, non-urbanized areas. Waterbirds 31:122–126. https://doi.org/10.1675/1524-4695(2008)31[122:SMDAFC]2.0.CO;2
Auman HJ, Bond AL, Meathrel CE, Richardson AMM (2011) Urbanization of the silver Gull: evidence of anthropogenic feeding regimes from stable isotope analyses. Waterbirds 34:70–76. https://doi.org/10.1675/063.034.0108
Barrett RT, Camphuysen K, Anker-Nilssen T et al (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691. https://doi.org/10.1093/icesjms/fsm152
Belant J. L (1997) Gulls in urban environments: landscape-level management to reduce conflict. Landsc Urban Plan 38:245–258. https://doi.org/10.1016/S0169-2046(97)00037-6
Belant J. L, Ickes S. K, Seamans T. W (1998) Importance of landfills to urban-nesting herring and ring-billed gulls. Landsc Urban Plan 43:11–19. https://doi.org/10.1016/S0169-2046(98)00100-5
Bellas J, Martínez-Armental J, Martínez-Cámara A, Besada V, Martínez-Gómez C (2016) Ingestion of microplastics by demersal fish from the Spanish Atlantic and Mediterranean coasts. Mar Pollut Bull 109:55–60. https://doi.org/10.1016/j.marpolbul.2016.06.026
Canestrelli A, Fraticelli F (2016) Yellow-legged Gull Larus michahellis captures and drowns a feral pigeon Columba livia. Riv Ital di Ornitol 69–69
Castillo-Contreras R, Carvalho J, Serrano E et al (2018) Urban wild boars prefer fragmented areas with food resources near natural corridors. Sci Total Environ 615:282–288. https://doi.org/10.1016/j.scitotenv.2017.09.277
Catry P, Matias R, Vicente L, Granadeiro JP (2009) Brood-guarding behaviour in Cory’s shearwaters Calonectris diomedea. J Ornithol 150:103–108. https://doi.org/10.1007/s10336-008-0322-x
Ceia F, Paiva V, Fidalgo V et al (2014) Annual and seasonal consistency in the feeding ecology of an opportunistic species, the yellow-legged gull Larus michahellis. Mar Ecol Prog Ser 497:273–284. https://doi.org/10.3354/meps10586
Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorial. PRIMER-E
Codina-García M, Militão T, Moreno J, González-Solís J (2013) Plastic debris in Mediterranean seabirds. Mar Pollut Bull 77:220–226. https://doi.org/10.1016/j.marpolbul.2013.10.002
Coulson JC, Coulson BA (2009) Ecology and colonial structure of large gulls in an urban Colony: investigations and Management at Dumfries, SW Scotland. Waterbirds 32:1–15. https://doi.org/10.1675/063.032.0101
Derraik J. G. (2002) The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull 44:842–852. https://doi.org/10.1016/S0025-326X(02)00220-5
Egbeocha C, Malek S, Emenike C, Milow P (2018) Feasting on microplastics: ingestion by and effects on marine organisms. Aquat Biol 27:93–106. https://doi.org/10.3354/ab00701
Fuirst M, Veit RR, Hahn M, Dheilly N, Thorne LH (2018) Effects of urbanization on the foraging ecology and microbiota of the generalist seabird Larus argentatus. PLoS One 13:e0209200. https://doi.org/10.1371/journal.pone.0209200
García S, Durany E (2005) La reintroducción del halcón peregrino en la ciudad de Barcelona: el sigiloso regreso de los halcones urbanos. Quercus 229:14–20
García-Petit J, Martí M. E, Tomas X, et al (1986) Colonització de la ciutat de Barcelona pel Gavia Argentat (Larus cachinnans). Miscel·lània Zoològica 10:401-403e
Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 25:90–98. https://doi.org/10.1016/j.tree.2009.07.016
Idescat (2019) Anuari estadístic de Catalunya. Pesca. Institut d'Estadística de Catalunya, Barcelona, Spain
Landfill Directive (1999) Council directive 1999/31/EC of 26 April 1999 on the landfill of waste. Official Journal of the European Communities, I. 182/1, Office for official publications of the European Communities, 2, rue Mercier, L – 2985 Luxembourg
Leveau LM (2018) Urbanization, environmental stabilization and temporal persistence of bird species: a view from Latin America. PeerJ 6:e6056. https://doi.org/10.7717/peerj.6056
Lim H. C, Sodhi N. S (2004) Responses of avian guilds to urbanisation in a tropical city. Landsc Urban Plan 66:199–215. https://doi.org/10.1016/S0169-2046(03)00111-7
Lopezosa P, Forero MG, Ramírez F, Navarro J (2019) Individuals within populations: no evidences of individual specialization in the trophic habits of an opportunistic predator. Estuar Coast Shelf Sci 229:106427. https://doi.org/10.1016/j.ecss.2019.106427
Marin G, Bettella E, Pilastro A et al (1995) Dependence of chick killing on nest density in a colony of yellow-legged gull (Larus cachinnans michaellis). Bolletino di Zool 62:9–11. https://doi.org/10.1080/11250009509356044
Matos DM, Ramos JA, Calado JG et al (2018) How fishing intensity affects the spatial and trophic ecology of two gull species breeding in sympatry. ICES J Mar Sci 75:1949–1964. https://doi.org/10.1093/icesjms/fsy096
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453
Mendes RF, Ramos JA, Paiva VH, Calado JG, Matos DM, Ceia FR (2018) Foraging strategies of a generalist seabird species, the yellow-legged gull, from GPS tracking and stable isotope analyses. Mar Biol 165:168–114. https://doi.org/10.1007/s00227-018-3421-0
Migura-Garcia L, Ramos R, Cerdà-Cuéllar M (2017) Antimicrobial resistance of Salmonella Serovars and Campylobacter spp. isolated from an opportunistic Gull species, yellow-legged Gull (Larus michahellis). J Wildl Dis 53:148–152. https://doi.org/10.7589/2016-03-051
Monaghan P (1979) Aspects of the breeding biology of herring gulls Larus argentatus in urban colonies. Ibis 121:475–481
Monaghan P (1982) The breeding ecology of urban nesting gulls. In: Bornkamm R, Lee JA, Seaward MRD (eds) Urban ecology: the second European ecological symposium, Berlin, 8–12 September 1980. Blackwell Scientific Publications, Oxford, pp 111–121
Navarro J, Grémillet D, Afán I, Ramírez F, Bouten W, Forero MG (2016) Feathered detectives: real-time GPS tracking of scavenging gulls pinpoints illegal waste dumping. PLoS One 11:e0159974. https://doi.org/10.1371/journal.pone.0159974
Navarro J, Grémillet D, Ramirez FJ, Afán I, Bouten W, Forero MG (2017) Shifting individual habitat specialization of a successful predator living in anthropogenic landscapes. Mar Ecol Prog Ser 578:243–251. https://doi.org/10.3354/meps12124
Navarro J, Grémillet D, Afán I, Miranda F, Bouten W, Forero MG, Figuerola J (2019) Pathogen transmission risk by opportunistic gulls moving across human landscapes. Sci Rep 9:10659. https://doi.org/10.1038/s41598-019-46326-1
Oro D, Genovart M, Tavecchia G et al (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16:1501–1514. https://doi.org/10.1111/ele.12187
Palomino D, Carrascal LM (2007) Habitat associations of a raptor community in a mosaic landscape of Central Spain under urban development. Landsc Urban Plan 83:268–274. https://doi.org/10.1016/j.landurbplan.2007.04.011
Passos C, Navarro J, Giudici A, González-Solís J (2010) Effects of extra mass on the pelagic behavior of a seabird. Auk 127:100–107. https://doi.org/10.1525/auk.2009.09036
Payo-Payo A, Oro D, Igual JM, Jover L, Sanpera C, Tavecchia G (2015) Population control of an overabundant species achieved through consecutive anthropogenic perturbations. Ecol Appl 25:2228–2239. https://doi.org/10.1890/14-2090.1
Phillips RA, Xavier JC, Croxall JP (2003) Effects of satellite transmitters on albatrosses and petrels. Auk 120:1082–1090
QGIS Development T (2019) QGIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
Ramírez F, Afán I, Bouten W, Carrasco JL, Forero MG, Navarro J (2020) Humans shape the year-round distribution and habitat use of an opportunistic scavenger. Ecol Evol. https://doi.org/10.1002/ece3.6226
Ramos R, Ramírez F, Sanpera C et al (2008) Diet of yellow-legged Gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: the relevance of refuse dumps. J Ornithol 150:265–272. https://doi.org/10.1007/s10336-008-0346-2
Ramos R, Ramírez F, Sanpera C et al (2009) Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods. Mar Ecol Prog Ser 377:289–297. https://doi.org/10.3354/meps07792
Rock P (2005) Urban gulls. Br Birds 98:338–355
Rock P, Camphuysen CJ, Shamoun-Baranes J et al (2016) Results from the first GPS tracking of roof-nesting herring gulls Larus argentatus in the UK. Ringing Migr 31:47–62. https://doi.org/10.1080/03078698.2016.1197698
Schwartz ALW, Williams HF, Chadwick E et al (2018) Roadkill scavenging behaviour in an urban environment. J Urban Ecol 4. https://doi.org/10.1093/jue/juy006
Senar JC, Arroyo L, Ortega-Segalerva A, Carrillo JG, Tomás X, Montalvo T, Sanz-Aguilar A (2019) Estimating age-dependent survival when juveniles resemble females: invasive ring-necked parakeets as an example. Ecol Evol 9:891–898. https://doi.org/10.1002/ece3.4366
Sol D, Senar J. C (1994) Ecologia del Gavià argentat: causas de la seva expansió i bases per a la planificació d’un programa de control. Barcelona, Spain
Sol D, Arcos J. M, Senar J. C (1993) Do yellow-legged gulls (Larus cachinnans) use refuse tips whenever they need to? Miscel·lània Zoològica 17:199–203
Sorace A, Gustin M (2009) Distribution of generalist and specialist predators along urban gradients. Landsc Urban Plan 90:111–118. https://doi.org/10.1016/j.landurbplan.2008.10.019
Sotillo A, Baert JM, Müller W, Stienen EWM, Soares AMVM, Lens L (2019) Recently-adopted foraging strategies constrain early chick development in a coastal breeding gull. PeerJ 7:e7250. https://doi.org/10.7717/peerj.7250
Spelt A, Williamson C, Shamoun-Baranes J, Shepard E, Rock P, Windsor S (2019) Habitat use of urban-nesting lesser black-backed gulls during the breeding season. Sci Rep 9:10527. https://doi.org/10.1038/s41598-019-46890-6
Thaxter CB, Ross-Smith VH, Clark JA et al (2014) A trial of three harness attachment methods and their suitability for long-term use on lesser black-backed gulls and great Skuas. Ringing Migr 29:65–76. https://doi.org/10.1080/03078698.2014.995546
Vázquez B, Esperón F, Neves E, López J, Ballesteros C, Muñoz MJ (2010) Screening for several potential pathogens in feral pigeons (Columba livia) in Madrid. Acta Vet Scand 52:45. https://doi.org/10.1186/1751-0147-52-45
Vergara A, Pitart C, Montalvo T, et al (2017) Prevalence of extended-spectrum-β-lactamase- and/or carbapenemase-producing Escherichia coli isolated from yellow-legged gulls from Barcelona, Spain. Antimicrob agents Chemother 61:AAC.02071-16. https://doi.org/10.1128/AAC.02071-16
Vidal E, Medail F, Tatoni T (1998) Is the yellow-legged gull a superabundantbird species in the Mediterranean? Impacton fauna and flora, conservation measuresand research priorities. Biodivers Conserv 7:1013–1026. https://doi.org/10.1023/A:1008805030578
Vincent T, Guiguen C (1989) Prédation sur des Pigeons domestiques Columba livia, par les Goélands, Larus argentatus et Larus cachinnans, et conséquences éventuelles pour la pathologie humaine. Nos Oiseaux 417:129–140
Washburn BE, Bernhardt GE, Kutschbach-Brohl L et al (2013) Foraging ecology of four Gull species at a coastal–urban Interface. Condor 115:67–76. https://doi.org/10.1525/cond.2013.110185
Wilcox C, Van Sebille E, Hardesty BD (2015) Threat of plastic pollution to seabirds is global, pervasive, and increasing. Proc Natl Acad Sci 112:11899–11904. https://doi.org/10.1073/pnas.1502108112
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JB, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790. https://doi.org/10.1126/science.1132294
Zorrozua N, Aldalur A, Herrero A et al (2020) Breeding yellow-legged gulls increase consumption of terrestrial prey after landfill closure. Ibis 162:50–62. https://doi.org/10.1111/ibi.12701
Acknowledgements
Thanks to the staff of the Zoo of Barcelona and the Institute of Marine Sciences - CSIC, especially Toni Lombarte, Sara Soto and Pablo Cermeño for their help in the otolith identification, spatial analysis and trapping procedures, respectively. All work procedures followed national and regional regulations. Sarah Young revised the English grammar. This study is part of the BCN-Gulls project funded by the Barcelona Zoo Foundation and the Ramón y Cajal project (RYC-2015-17809) led by J.N. This study is part of the Master’s thesis of A.M. All fieldwork was conducted in accordance with the Spanish and EU legislation on the protection of animals used for scientific purposes.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Electronic supplementary material
ESM 1
(DOCX 2583 kb)
Rights and permissions
About this article
Cite this article
Méndez, A., Montalvo, T., Aymí, R. et al. Adapting to urban ecosystems: unravelling the foraging ecology of an opportunistic predator living in cities. Urban Ecosyst 23, 1117–1126 (2020). https://doi.org/10.1007/s11252-020-00995-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11252-020-00995-3